- Signalling theory
evolutionary biology, signalling theory refers to a body of theoretical work examining communication between individuals. The central question is when animals with conflicting interests should be expected to communicate "honestly". Mathematical modelsin which organisms signal their condition to other individuals as part of an evolutionarily stable strategyare the principal form of research in this field.
In biology, signals are traits, including structures and behaviors, that have evolved specifically because they change the behavior of receivers in ways that benefit the signaler [ Bradbury, J.W. & S.L. Vehrenkamp (1998) Principles of animal communication. Sinauer, Sunderland (MA) ] . Traits or actions that benefit the receiver exclusively are called cues. When an alert bird deliberately gives a warning call to a stalking predator and the predator gives up the hunt, the sound is a signal. When a foraging bird inadvertently makes a rustling sound in the leaves that attracts predators and increases the risk of predation, the sound is a cue.
Signaling systems are shaped by the extent to which signalers and receivers have mutual interests. An alert bird warning off a stalking predator is communicating something useful to the predator: that it has been detected by the prey; it might as well quit wasting its time stalking this alerted prey, which it is unlikely to catch. When the predator gives up, the signaler can get back to other important business. Once the stalking predator is detected, the signaling prey and receiving predator have a mutual interest terminating the hunt [ Bergstrom, C.T. & M. Lachmann (2001) Alarm calls as costly signals of antipredator vigilance: the watchful babbler game. Anim. Behav. 61, 535-543 ] [ Getty, T. (2002) The discriminating babbler meets the optimal diet hawk. Anim. Behav. 63, 397-402 ] .
Within species, mutual interests generally increase with kinship [ Johnstone, R.A. (1998) Conspiratorial whispers and conspicuous displays: Games of signal detection. Evolution 52, 1554-1563 ] . Kinship is central to models of signaling between relatives, for instance when broods of nestling birds beg and compete for food from their parents [ Godfray, H.C.J. (1995) Evolutionary theory of parent-offspring conflict. Nature 376, 133 ] [ Johnstone, R.A. (2002) Signalling of need, sibling competition, and the cost of signaling. Proc. Nat’l. Acad. Sci. USA 96, 12644-12649 ] . The distinction between signals and cues is not clear, and probably not useful for immune, endocrine and neural signaling between the cells within an individual, at least to the extent that all of these cells are clonal descendents of a fertilized egg and there are no conflicts of interest between them. The concept of honesty in animal communication is controversial because it is difficult to determine intent and use that as a criterion to discriminate deception from honesty, as we do in human interactions [ Getty, T. (1997) Deception: the correct path to enlightenment? Trends Ecol. & Evol. 12, 159-160 ] . Because of this, biologists who use the phrase ”honest signals” use it in a statistical sense. Biological signals, like warning calls or resplendent tail feathers, are considered honest if they are correlated with, or reliably predict, something useful to the receiver. In this usage, honesty is a useful correlation between the signal trait (which economists call ”public information” because it is readily apparent) and the unobservable thing of value to the receiver (which economists refer to as “private information” and biologists often refer to as “quality”). Honest biological signals do not need to be perfectly informative, reducing uncertainty to zero; they only need to be honest “on average” to be potentially useful [ Johnstone, R.A. & A. Grafen (1993) Dishonesty and the handicap principle, Anim Behav. 46, 759-764 ] . Ultimately the value of the signaled information depends on the extent to which it allows the receiver to increase its fitness [ Dall, S.R.X. (2005) Information and its use by animals in evolutionary ecology. Trends Ecol. & Evo. 20, 187-193 ] Because there are both mutual and conflicting interests in most animal signaling systems, the fundamental problem in evolutionary signaling games is dishonesty or cheating. Why don’t foraging birds just give warning calls all the time, at random (false alarms), just in case a predator is nearby? If peacocks with bigger tails are preferred by peahens, why don’t all peacocks display big tails? Too much cheating would disrupt the correlation at the foundation of the system, causing it to collapse. Receivers should ignore the signals if they are not useful to them and signalers shouldn’t invest in costly signals if they won’t alter the behavior of receivers in ways that benefit the signaler. What prevents cheating from destabilizing signaling systems? It might be apparent that the costs of displaying signals must be an important part of the answer. However, understanding how costs can stabilize an “honest” correlation between the public signal trait and the private signaled quality has turned out to be a long, interesting process.
The question of whether individuals of the same species might not be attempting to deceive each other was raised by
Richard Dawkinsand John Krebsin 1978. This thinking was prompted by the application of a gene-centered view of evolutionto the use of threat displays. Dawkins & Krebs criticised previous ethologists, such as Nikolaas Tinbergenand Desmond Morrisamong others, for supporting the view that such displays were used "for the good of the species". Dawkins and Krebs (and Krebs and Dawkins, 1982) argued that such communication ought to be viewed as an evolutionary arms racein which signallers evolve to become better at manipulating receivers, while receivers evolve to become more resistant to manipulation.
The game theoretical model of the war of attrition was applied to the problem, and appeared to suggest that threat displays ought not to convey any reliable information about intentions (Caryl, 1979). This led to a re-examination of the empirical evidence, and much debate Fact|date=February 2007.
The Sports Handicapping Metaphor
Amotz Zahaviproposed a verbal model for how signal costs could constrain cheating and stabilize an “honest” correlation between observed signals and unobservable qualities, based on an analogy to sports handicapping systems [ Zahavi, A. (1975) Mate selection – selection for a handicap. J. Theor. Biol. 53, 205–214 ] Zahavi, A. and Zahavi, A. (1997) The Handicap Principle, Oxford University Press ] . He called this idea the handicap principle. The purpose of a sports handicapping system is to reduce disparities in performance, making the contest more competitive. In horse racing, intrinsically faster horses are given heavier weights to carry under their saddles. In amateur golf , better golfers have fewer strokes subtracted from their raw scores. This creates correlations between the handicap and unhandicapped performance, and if the handicaps work as they are supposed to, between the handicap and handicapped performance. If you knew nothing about two race horses or two amateur golfers except their handicaps, you could infer which horse or golfer has had the better performance in the recent past, and you should expect the competitors with the biggest handicaps to win. By analogy, if peacock tails act as a handicapping system, and a peahen knew nothing about two peacocks but the sizes of their tails, she could “infer” that the peacock with the bigger tail has greater unobservable intrinsic quality, in the sense that it is better able to pay the costs of displaying the tail (here, “infer” is shorthand for the idea that females that prefer bigger tails are at a selective advantage). Display costs can include extrinsic social costs, in the form of testing and punishment by rivals, as well as intrinsic production costs [ Searcy, W.A. & S. Nowicki (2005) The evolution of animal communication: reliability and deception in signaling systems. Princeton University Press, Princeton (NJ) ] .
The essential idea here is intuitive and probably qualifies as folk wisdom. It was articulated quite nicely by
Kurt Vonnegut, in his 1961 short story Harrison Bergeron[ Vonnegut, K. (1961) Harrison Bergeron. Fan. Sci. Fict. Mag. Oct., 5–10 ] . In Vonnegut’s futuristic dystopia, the Handicapper General uses a variety of handicapping mechanisms to reduce inequalities in performance. A spectator at a ballet comments: “it was easy to see that she was the strongest and most graceful of all dancers, for her handicap bags were as big as those worn by two hundred pound men.” Zahavi interpreted this analogy to mean that higher quality peacocks with bigger tails are signaling their ability to "waste" more of something important by trading it off for a bigger tail. This resonates with Veblen’s idea that conspicuous consumptionand extravagant status symbols can signal wealth [ Veblen, T. (1899) The Theory of the Leisure Class: an Economic Study of Institutions, Penguin ] . One area where there is currently a lot of research on this idea involves the duel roles of carotenoid pigments in immune system function and in yellow-red bird feathers [ McGraw, K.J. & D. R. Ardia (2003) Carotenoids, immunocompetence, and the information content of sexual colors: An experimental test. Am. Nat. 162, 704-712 ] . Carotenoids have to be ingested because animals cannot synthesize them de novo. It is hypothesized that birds with redder feathers are demonstrating their ability to “waste” more carotenoids by allocating them to feathers rather than to immune function. The red feathers are hypothesized to be an immunocompetence handicap [ Folstad, I. & A.J. Karter (1992) Parasites, bright males, and the immunocompetence handicap. Am. Nat. 139, 603-622 ] .
Zahavi’s conclusions rest on his verbal interpretation of a metaphor, and initially, the handicap principle was not well received by evolutionary biologists Z&Z97] . However, in 1984, Nur and Hasson Nur, N. and Hasson, O. (1984) Phenotypic plasticity and the handicap principle. J. Theor. Biol. 110, 275–297 ] used life history theory to show how differences in signaling costs, in the form of survival-reproduction tradeoffs, could stabilize a signaling system roughly as Zahavi imagined. Later in the decade, several papers using genetic models also began to suggest that the idea just might work, at least some times McElreath, R & R. Boyd. (2007) Mathematical Models of Social Evolution. Univ. Chicago Press, Chicago ] . The logjam was broken in 1990 by Alan Grafen, Grafen, A. (1990) Biological signals as handicaps. J. Theor. Biol. 144, 517–546 ] who developed a very complicated marginal fitness maximization model of evolutionary signaling games and came to the conclusion that, given certain assumptions, a handicap-like signaling system could be evolutionarily stable, if higher quality signalers paid lower marginal survival costs for their signals. This, and the seminal paper by W. D. Hamilton and Zuk [ Hamilton, W.D. and Zuk, M. (1982) Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387 ] suggesting that sexually selected signals are signals of health, in a never-ending co-evolutionary race between hosts and their parasites, led to an explosion of research on the relationship between sexually selected signals, parasites and mate preferences.
Re-evaluating Biological Signaling vs. Sports Handicapping
Efforts to test the handicap principle empirically have not been decisive, partly because of inconsistent interpretations of Zahavi’s metaphor and Grafen’s marginal fitness model, and partly because of conflicting empirical results: in some studies individuals with bigger signals seem to be paying higher costs, in other studies they seem to be paying lower costs [ Møller, A. P., P. Christe, & E. Lux (1999) Parasitism, host immune function, and sexual selection. Quarterly Review of Biology 74, 3–20 ] [ Kotiaho, J.S. (2001) Costs of sexual traits: a mismatch between theoretical considerations and empirical evidence. Biological Reviews 76, 365-376 ] . Recent theoretical analyses have uncovered a possible explanation for the inconsistent empirical results. A series of papers by Getty [ Getty, T. (1998) Handicap signalling: when fecundity and viability do not add up. Anim. Behav. 56, 127–130 ] [ Getty, T. (1998) Reliable signalling need not be a handicap. Anim. Behav. 56, 253–255 ] [ Getty, T. (2002) Signaling health versus parasites. Am. Nat. 159,363–371 ] Getty. T (2006) Sexually selected signals are not similar to sports handicaps. Trends Ecol. & Evol 21, 83-88 ] shows that Grafen’s proof of the handicap principle is based on the critical simplifying assumption that signalers trade off costs for benefits in an additive fashion, the way humans invest money to increase income in the same currency. Grafen’s proof is formally similar to a classic monograph on economic market signaling by Nobel laureate
Michael Spence[ Spence, A.M. (1974) Market Signaling, Information Transfer in Hiring and Related Processes, Harvard University Press ] . This assumption that costs and benefits trade off in an additive fashion might be valid for some biological signaling systems, but is not valid for the survival cost – reproduction benefit tradeoff that is assumed to mediate the evolution of sexually selected signals. Fitness depends on the production of offspring and this is a multiplicative function of reproductive success given an individual is still alive times the probability of still being alive, given investment in signals N&H84] . Survival-reproduction tradeoffs do not correspond to sports handicaps in any simple, useful way. Zahavi’s intuition was correct in the very general sense that “differences in costs” can stabilize the evolution of an “honest” signaling system, but in sexually selected signaling, “differences in costs” are properly decreasing proportional (or log) marginal costs Getty06] . The mathematics can be interpreted to mean that higher quality signalers are more efficient at converting signal costs into reproductive benefits. This re-analysis undermines the idea that higher quality signalers are demonstrating their ability to waste more because the pattern of absolute signal costs across signalers of different quality remains undetermined. Depending on the specific form of the tradeoffs in any particular system, higher quality signalers might pay absolutely more or less for big signals than lower quality signalers pay for small signals. This might explain why the empirical data on the relationship between signals and costs are so inconsistent.
Costly Signaling and Fisherian Diploid Dynamics
The effort to discover how costs can constrain an “honest” correlation between public signals and private qualities within signalers is built on strategic models of signaling games, with many simplifying assumptions. These models are most often applied to sexually selected signaling in
diploidanimals, but they rarely incorporate an important feature of diploid sexual reproduction that was pointed out by Ronald Fisher in the early 20th century: if there are “preference genes” correlated with choosiness in females as well as “signal genes” correlated with display traits in males, choosier females should tend to mate with showier males. Over generations, showier sons should also carry genes associated with choosier daughters and choosier daughters should also carry genes associated with showier sons. This correlation could introduce an evolutionary dynamic known as a Fisherian runaway. Russell Lande explored this with quantitative genetic models and his work inspired a very active line of research in the quantitative genetic framework M&B07] . These analyses revealed that Fisherian diploid dynamics are very sensitive to signaling and search costs. Recent models have begun to bridge the gap between the costly-signaling and Fisherian-runaway traditions by developing modeling frameworks that incorporate both simultaneously [ Eshel, I. et al. (2002) A long-term genetic model for the evolution of sexual preference: the theories of Fisher and Zahavi re-examined. J. Math. Biol. 45, 1–25 ] [ Kokko, H. et al. (2002) The sexual selection continuum. Proc. Roy. Soc. Lond. B. 269, 1331-1340 ] . These models recognize that if fitness depends on both survival and reproduction, having sexy sons and choosy daughters (in the stereotypical model) can be adaptive, increasing fitness just as much as having healthy sons and daughters.
* Sam Brown and
W.D. Hamilton[ Hamilton and Brown (2001) [http://cluster3.biosci.utexas.edu/research/meyers/SamB/HamiltonBrown01.pdf Autumn tree colours as a handicap signal. PDF] Proc. R. Soc. B 268:1489-1493 ] and Marco Archetti [ Archetti (2000) [http://users.ox.ac.uk/~zool0643/papers/JTB_2000_autumn.pdf The origin of autumn colours by coevolution. PDF] J. Theor. Biol. 205: 625-630 ] proposed the idea that Autumn leaf coloris due to the trees signalling to aphids and other pest species that migrate to the trees in autumn. Autumn colour is costly to trees but bright trees might reduce their parasite load; aphids on the other hand might prefer trees with dull leaves because these are the ones with less chemical defenses. Indeed aphids appear to preferentially avoid trees with bright leaves and tree species with bright leaves have more specialist aphid pests than do trees lacking bright leaves. While autumn colours might be a real handicap signal, it is not necessary that the signal is costly to produce. It might also be an index, which is maintained because it is impossible to fake (it would be a signal instead if only strong individuals can afford the cost of displaying it). The topic is still debated.
Stottingfor example in Thomson's Gazelles is cited as an example of signaling: the gazelles jump close to a predator instead of escaping, in what could be a signal of strength.
Human Honest Signals
Because honest signals are found in a wide variety of species it is reasonable to expect that humans have also evolved honest signals. Examples of human honest signals that have been suggested include neonatal cry quality as a signal that promotes neonatal survival(Madkour et al 1997), increases in activity level (e.g., autonomic nervous system arousal) as a signal that promotes changes in group activity level through mood contagion, or verbal and postural mirroring as a signal that promotes feelings of trust and empathy in others (Pentland 2008). Evidence from behavioral economics show that changes in arousal, trust or empathy also change individual assessments of risk and reward. More abstract honest signals have also been suggested, including the General Intelligence factor (g) as a signal of fitness (Luxen and Buunk 2006) and key features of human language (Lachmann et al 2001).
Autumn leaf color
* Archetti M. 2000 The origin of autumn colours by coevolution. "J. Theor. Biol." 205: 625-630.
* Caryl, P. G. 1979: Communication by agonistic displays: what can games theory contribute to ethology? "Behaviour" 68:136-169.
* Dawkins, R. & Krebs, J. R. 1978: Animal signals: information or manipulation? in "Behavioural Ecology: an evolutionary approach" 1st ed. (Krebs, J. R. & ,Davies, N.B., eds) Blackwell: Oxford, pp 282-309.
* Enquist, M. 1985: Communication during aggressive interactions with particular reference to variation in choice of behaviour. "Animal Behaviour" 33, 1152-1161.
* Grafen, A. 1990: Biological signals as handicaps. "Journal of Theoretical Biology" 144: 517-546.
* Hamilton, W.D. & Brown, S.P. 2001 Autumn tree colours as a handicap signal. "Proc. R. Soc. B" 268:1489-1493.
* Kirkpatrick, M 1986: The handicap mechanism of sexual selection does not work. "American Naturalist" 127, 222-240.
* Krebs, J. R. and Dawkins, R. 1984: Animal signals: mind-reading and manipulation. in "Behavioural Ecology: an evolutionary approach", 2nd ed (Krebs, J. R. & ,Davies, N.B., eds), Sinauer: pp 380-402
* Lachmann, M., Szamado, S., and Bergstrom, C.T., 2001: Cost and Conflict in animal signals and human language, PNAS, 98(23) 13189-13194
* Luxen, M.F., and Buunk, B.P., 2006: Human Intelligence, fluctuating asymmetry and the peacock’s tail: General Intelligence (g) as an honest signal of fitness, Personality & Individual Differencces, 41(5) 897-902
* Madkour, T.M., Barakat, A.M., and Furlow, F.B., 1997: Neonatal cry quality as an honest signal of fitness, Evolution & Human Behavior, 18(3) 175-193
* Maynard Smith, J. 1994: Must reliable signals always be costly? "Animal Behaviour" 47, 1115-1120.
* Maynard Smith, J and Harper, D. 2004: "Animal Signals"
* Pentland, A., 2008: Honest Signals: how they shape our world, MIT Press
* Zahavi, A. 1975: Mate selection — a selection for a handicap. Journal of theoretical Biology. 53, 205-214
* Zahavi, A. 1977: The cost of honesty (Further remarks on the handicap principle). Journal of theoretical Biology. 67, 603-605
* [http://octavia.zoology.washington.edu/handicap/ An Introduction to the Theory of Honest Signalling]
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